All 4 di-leucine motifs in the first hydrophobic domain of the E5 oncoprotein of human papillomavirus type 16 are essential for surface MHC class I downregulation activity and E5 endomembrane localization

International Journal of Cancer

Volumn 126, Issue 7, 2010, Pages 1675-1682

  Cortese, Marc S ^a   Ashrafi, G Hossein ^a,b   Campo, M Saveria ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b KINGSTON UNIVERSITY   (United Kingdom)

Author keywords

Bap31; Di leucine motifs; HPV 16 E5 oncoprotein; Immunomodulation; Major histocompatibility complex class I; Molecular interactions

Indexed keywords

LEUCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEMBRANE PROTEIN; ONCOPROTEIN; ONCOPROTEIN E5; UNCLASSIFIED DRUG; VALINE; HLA ANTIGEN CLASS 1; MESSENGER RNA; ONCOGENE PROTEIN E5, HUMAN PAPILLOMAVIRUS TYPE 16;

ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HYDROPHOBICITY; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SURFACE PROPERTY; CELL CULTURE; CHEMISTRY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSCRIPTION; GENETICS; IMMUNOPRECIPITATION; INTRACELLULAR MEMBRANE; KERATINOCYTE; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMINO ACID MOTIFS; CELLS, CULTURED; DOWN-REGULATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMAN PAPILLOMAVIRUS 16; HUMANS; HYDROPHOBICITY; IMMUNOPRECIPITATION; INTRACELLULAR MEMBRANES; KERATINOCYTES; LEUCINE; MUTATION; ONCOGENE PROTEINS, VIRAL; PROTEIN BIOSYNTHESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 77449148386     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25004     Document Type: Article

References (29)

1. O'Brien PM, Campo MS. Evasion of host immunity directed by papillomavirus-encoded proteins. Virus Res 2002;88: 103-17.
2. zur Hausen H. Papillomaviruses in the causation of human cancers-a brief historical account. Virology 2009;384:260-5.
3. Ashrafi GH, Haghshenas MR, Marchetti B, O'Brien PM, Campo MS. E5 protein of human papillomavirus type 16 selectively down-regulates surface HLA Class I. Int J Cancer 2005;113:276-83.
4. Ashrafi GH, Haghshenas MR, Marchetti B, Campo MS. E5 protein of Human Papillomavirus 16 down-regulates HLA Class I and interacts with the heavy chain via its first hydrophobic domain. Int J Cancer 2006;119:2105-12.
5. Fehrmann F, Klumpp DJ, Laimins LA. Human papillomavirus type 31 E5 protein supports cell cycle progression and activates late viral functions upon epithelial differentiation. J Virol 2003;77:2819-31.
6. Genther SM, Sterling S, Duensing S, Munger K, Sattler C, Lambert PF. Quantitative role of the human papillomavirus type 16 E5 gene during the productive stage of the viral life cycle. J Virol 2003;77:2832-42.
7. Suprynowicz FA, Campo MS, Schlegel R. Biological activities of papillomavirus E5 proteins. In: Campo MS, ed. Papillomavirus Research: From Natural History to Vaccines and Beyond, Caister Academic Press, Norfolk, UK, 2006. 97-113.
8. Leechanachai P, Banks L, Moreau F, Matlashewski G. The E5 gene from human papillomavirus type 16 is an oncogene which enhances growth factor-mediated signal transduction to the nucleus. Oncogene 1992;7:19-25.
9. Genther Williams SM, Disbrow GL, Schlegel R, Lee D, Threadgill DW, Lambert PF. Requirement of epidermal growth factor receptor for hyperplasia induced by E5, a high-risk human papillomavirus oncogene. Cancer Res 2005; 65:6534-42.
10. Ashrafi GH, Brown D, Fife KH, Campo MS. Down-regulation of MHC Class I is a property common to papillomavirus E5 proteins. Virus Res 2006;120:208-11.
11. Cartin W, Alonso A. The human papillomavirus HPV2a E5 protein localizes to the Golgi apparatus and modulates signal transduction. Virology 2003;314: 572-9.
12. Nath R, Mant C, Kell B, Cason J, Bible J. Analyses of variant human papillomavirus type-16 E5 proteins for their ability to induce mitogenesis of murine fibroblasts. Cancer Cell Int 2006;6:19.
13. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001;305: 567-80.
14. Raff T, van der Giet M, Endemann D, Wiederholt T, Paul M. Design and testing of beta-actin primers for RT-PCR that do not co-amplify processed pseudogenes. Biotechniques 1997;23: 456-60.
15. Marchetti B, Ashrafi GH, Araibi EH, Ellis SA, Campo MS. The E5 protein of BPV-4 interacts with the heavy chain of MHC Class I and irreversibly retains the MHC complex in the Golgi apparatus. Oncogene 2006;27:2254-63.
16. Ladasky JJ, Boyle S, Seth M, Li H, Pentcheva T, Abe F, Steinberg SJ, Edidin M. Bap31 enhances the endoplasmic reticulum export and quality control of human Class I MHC molecules. J Immunol 2006;177:6172-81.
17. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S, Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 2004; 86:3993-4003.
18. Lewis C, Baro MF, Marques M, Grüner M, Alonso A, Bravo IG. The first hydrophobic region of the HPV16 E5 protein determines protein cellular location and facilitates anchorage-independent growth. Virol J 2008;5:30-40.
19. Barbaresi S, Cortese MS, Quinn J, Ashrafi GH, Graham SV, Campo MS. Effects of human papillomavirus type 16 mutants on epithelial morphology: functional characterisation of each transmembrane domain. J Gen Virol 2010;91: in press [Epub ahead of print].
20. Bible JM, Mant C, Best JM, Kell B, Starkey WG, Shanti RK, Seed P, Biswas C, Muir P, Banatvala JE, Cason J. Cervical lesions are associated with human papillomavirus type 16 intratypic variants that have high transcriptional activity and increased usage of common mammalian codons. J Gen Virol 2000;81:1517-27.
21. Chan SY, Ho L, Ong CK, Chow V, Drescher B, Durst M, Ter Meulen J, Villa L, Luande J, Mgaya HN. Molecular variants of human papillomavirus type 16 from 4 continents suggest ancient pandemic spread of the virus and its coevolution with humankind. J Virol 1992; 66:2057-66.
22. Chen Z, Terai M, Fu L, Herrero R, DeSalle R, Burk RD. Diversifying selection in human papillomavirus type 16 lineages based on complete genome analyses. J Virol 2005;79:7014-23.
23. Eriksson A, Herron JR, Yamada T, Wheeler CM. Human papillomavirus type 16 variant lineages characterized by nucleotide sequence analysis of the E5 coding segment and the E2 hinge region. J Gen Virol 1999;80 (Part 3): 595-600.
24. Auvinen E, Alonso A, Auvinen P. Human papillomavirus type 16 E5 protein colocalizes with the antiapoptotic Bcl-2 protein. Arch Virol 2004;149:1745-59.
25. Gruener MBI, Momburg F, Alonso A, Tomakidi P. The E5 protein of the human papillomavirus type 16 down-regulates HLA-I surface expression in calnexinexpressing but not in calnexin-deficient cells. Virol J 2007;4:116.
26. Reusch U, Muranyi W, Lucin P, Burgert HG, Hengel H, Koszinowski UH. A cytomegalovirus glycoprotein re-routes MHC Class I complexes to lysosomes for degradation. EMBO J 1999;18:1081-91.
27. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003;72:395-447.
28. Regan JA, Laimins LA. Bap31 is a novel target of the human papillomavirus E5 protein. J Virol 2008;82:10042-51.
29. Senes A, Gerstein M, Engelman DM. Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J Mol Biol 2000;296:921-36.